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Positive feedback with mycorrhizal fungi alleviates negative effects of intercropping the energy crop Jatropha curcas with Crotalaria retusa

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Abstract

Little is known about the arbuscular mycorrhizal status of the ligneous plant Jatropha curcas, an energy crop that raises high expectations worldwide. We hypothesized that its early mycorrhization and growth could be improved by co-culturing it with Crotalaria retusa, a mycotrophic legume species. Soil samples collected from a 15-year-old J. curcas hedgerow were transferred to the greenhouse, along with soil sampled from the contiguous fallow field. Three pot-culture modalities were studied for 3 months: jatropha alone, jatropha sowed after the clipping of 2-month-old C. retusa, and jatropha sowed next to 2-month-old C. retusa. J. curcas biomass was significantly lower when it was co-cultured with C. retusa in both soil types as compared to when it was grown individually, while its biomass following the cut of C. retusa was not impacted. J. curcas shoot P content was significantly improved only when both plant species grew in the hedgerow soil, and so was mycorrhization intensity. Additionally, the composition of the J. curcas root mycorrhizal community was closer to that of C. retusa when using this hedgerow soil. Overall, J. curcas development was not improved by its association with C. retusa, but the soil cropping history appeared essential to their mycorrhizal interactions. These were favored by a soil mycorrhizal community shaped by multiple years of J. curcas monoculture. Improved knowledge about these preferential association patterns with J. curcas is needed to improve its co-culture with compatible mycotrophic legumes.

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References

  • Ae N, Arihara J, Okada K, Yoshihara T, Johansen C (1990) Phosphorus uptake by pigeon pea and its role in cropping systems of the Indian subcontinent. Science 248:477–480

    Article  CAS  PubMed  Google Scholar 

  • Aristizábal C, Rivera EL, Janos DP (2004) Arbuscular mycorrhizal fungi colonize decomposing leaves of Myrica parvifolia. M pubescens and Paepalanthus sp Mycorrhiza 14:221–228

  • Bainard LD, Klironomos JN, Hart MM (2010) Differential effect of sample preservation methods on plant and arbuscular mycorrhizal fungal DNA. J Microbiol Methods 82:124–130

    Article  CAS  PubMed  Google Scholar 

  • Brooker RW, Maestre FT, Callaway RM et al (2008) Facilitation in plant communities: the past, the present, and the future. J Ecol 96:18–34

    Article  Google Scholar 

  • Brooker RW, Bennett AE, Cong WF et al (2015) Improving intercropping: a synthesis of research in agronomy, plant physiology and ecology. New Phytol 206:107–117

    Article  PubMed  Google Scholar 

  • Brundrett MC, Abbott LK, Jasper DA (1999) Glomalean mycorrhizal fungi from tropical Australia I. Comparison of the effectiveness and specificity of different isolation procedures Mycorrhiza 8:305–314

    Google Scholar 

  • Callaway RM (1995) Positive interactions among plants. Bot Rev 61:306–348

    Article  Google Scholar 

  • Callaway RM, Walker LR (1997) Competition and facilitation: a synthetic approach to interactions in plant communities. Ecology 78:1958–1965

    Article  Google Scholar 

  • Campbell D (2014) Hope or hype: a critical assessment of Jatropha curcas for domestic biofuel production in Senegal. Dissertation, Victoria University of Wellington, New Zealand

    Google Scholar 

  • Chapagain T, Riseman A (2015) Nitrogen and carbon transformations, water use efficiency and ecosystem productivity in monocultures and wheat-bean intercropping systems. Nutr Cycl Agroecosyst 101:107–121

    Article  CAS  Google Scholar 

  • Daimon H, Kotoura S (2000) Incorporation of Crotalaria spectabilis grown at a high seeding rate inhibits the growth of the succeeding wheat crop. J Agron Crop Sci 185:137–144

    Article  Google Scholar 

  • Dieng A, Ndoye I, Duponnois R, Baudoin E (2014) Effects of Jatropha curcas L. Plantation on soil bacterial and fungal communities. Soil Biol Biochem 72:105–115

    Article  CAS  Google Scholar 

  • Dieng A, Ndoye I, Duponnois R, Baudoin E (2015) Cultivation of Jatropha curcas L. Leads to pronounced mycorrhizal community differences. Soil Biol Biochem 89:1–11

    Article  CAS  Google Scholar 

  • Edel-Hermann V, Dreumont C, Pérez-Piquerez A, Steinberg C (2004) Terminal restriction fragment length polymorphism analysis of ribosomal RNA genes to assess changes in fungal community structure in soils. FEMS Microbiol Ecol 47:397–404

    Article  CAS  PubMed  Google Scholar 

  • Edrisi SA, Dubey RK, Tripathi V, Bakshi M, Srivastava P, Jamil S, Singh HB, Singh N, Abhilash PC (2015) Jatropha curcas L.: a crucified plant waiting for resurgence. Renew Sust Energ Rev 41:855–862

    Article  Google Scholar 

  • Fischler M, Wortmann CS, Feil B (1999) Crotalaria (C. ochroleuca G. Don) as a green manure in maize-bean cropping systems in Uganda. Field Crop Res 61:97–107

    Article  Google Scholar 

  • Fitter AH, Graves JD, Watkins NK, Robinson D, Scrimgeour C (1998) Carbon transfer between plants and its control in networks of arbuscular mycorrhizas. Funct Ecol 12:406–412

    Article  Google Scholar 

  • Frey B, Schüepp H (1992) Transfer of symbiotically fixed nitrogen from berseem (Trifolium alexandrinum L.) to maize via vesicular-arbuscular mycorrhizal hyphae. New Phytol 122:447–454

    Article  CAS  Google Scholar 

  • Germani G, Plenchette C (2004) Potential of Crotalaria species as green manure crops for the management of pathogenic nematodes and beneficial mycorrhizal fungi. Plant Soil 266:333–342

    Article  CAS  Google Scholar 

  • Hammer EC, Pallon J, Wallander H, Olsson PA (2011) Tit for tat? A mycorrhizal fungus accumulates phosphorus under low plant carbon availability. FEMS Microbiol Ecol 76:236–244

    Article  CAS  PubMed  Google Scholar 

  • Hauggaard-Nielsen H, Jensen ES (2005) Facilitative root interactions in intercrops. Plant Soil 274:237–250

    Article  CAS  Google Scholar 

  • He XH, Critchley C, Bledsoe C (2003) Nitrogen transfer within and between plants through common mycorrhizal networks (CMNs). Crit Rev Plant Sci 22:531–567

    Article  Google Scholar 

  • Helgason T, Daniell TJ, Husband R, Fitter AH, Young JPW (1998) Ploughing up the wood-wide web ? Nature. doi:10.1038/28764

    PubMed  Google Scholar 

  • Hodge A, Campbell C, Fitter AH (2001) An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413:297–299

    Article  CAS  PubMed  Google Scholar 

  • Iiyama M, Newman D, Munster C, Nyabenge M, Sileshi GW, Moraa V, Onchieku J, Mowo JG, Jamnadass R (2013) Productivity of Jatropha curcas under smallholder farm conditions in Kenya. Agrofor Syst 87:729–746

    Article  Google Scholar 

  • Jensen ES (1996) Barley uptake of N deposited in the rhizosphere of associated field pea. Soil Biol Biochem 28:159–168

    Article  CAS  Google Scholar 

  • Johansen A, Jensen ES (1996) Transfer of N and P from intact or decomposing roots of pea to barley interconnected by an arbuscular mycorrhizal fungus. Soil Biol Biochem 28:73–81

    Article  CAS  Google Scholar 

  • Jourand P, Rapior S, Fargette M, Mateille T (2004) Nematostatic activity of aqueous extracts of west African Crotalaria species. Nematology 6:765–771

    Article  Google Scholar 

  • Klironomos JN, Hart MM (2002) Colonization of roots by arbuscular mycorrhizal fungi using different sources of inoculum. Mycorrhiza 12:181–184

  • Lee J, Lee S, Young JPW (2008) Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiol Ecol 65:339–349

    Article  CAS  PubMed  Google Scholar 

  • Li L, Li SM, Sun JH, Zhou LL, Bao XG, Zhang HG, Zhang FS (2007) Diversity enhances agricultural productivity via rhizosphere phosphorus facilitation on phosphorus-deficient soils. Proc Natl Acad Sci U S A 104:11192–11196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Ran W, Zhang R, Sun S, Xu G (2009) Facilitated legume nodulation, phosphate uptake and nitrogen transfer by arbuscular inoculation in an upland rice and mung bean intercropping system. Plant Soil 315:285–296

    Article  CAS  Google Scholar 

  • Li L, Tilman D, Lambers H, Zhang FS (2014) Plant diversity and overyielding: insights from belowground facilitation of intercropping in agriculture. New Phytol 203:63–69

    Article  PubMed  Google Scholar 

  • Matos FS, Carvalho DDC, ACde S, TG N, RP R, CKL C, VdoR R, PGdeF S (2014) Agronomic feasibility of the intercropping Jatropha curcas L. And Glycine max L. Rev Agr 7:226–232

    Google Scholar 

  • Meng L, Zhang A, Wang F, Han X, Wang D, Li S (2015) Arbuscular mycorrhizal fungi and rhizobium facilitate nitrogen uptake and transfer in soybean/maize intercropping system. Front Plant Sci. doi:10.3389/fpls.2015.00339

    Google Scholar 

  • Openshaw K (2000) A review of Jatropha curcas: an oil plant of unfulfilled promise. Biomass Bioenergy 19:1–15

    Article  Google Scholar 

  • Pandey A, Singh R, Sharma SK, Bhandari DC (2010) Diversity assessment of useful Crotalaria species in India for plant genetic resources management. Genet Resour Crop Evol 57:461–470

    Article  Google Scholar 

  • Paynel F, Murray PJ, Cliquet JB (2001) Root exudates: a pathway for short-term N transfer from clover and ryegrass. Plant Soil 229:235–243

    Article  CAS  Google Scholar 

  • Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. T Brit Mycol Soc 55:158–161

    Article  Google Scholar 

  • Postma JA, Lynch JP (2012) Complementarity in root architecture for nutrient uptake in ancient maize/bean and maize/bean/squash polycultures. Ann Bot-London 110:521–534

    Article  CAS  Google Scholar 

  • Renner A, Zelt T, Gerteiser S (2008) Global market study on jatropha. Final report prepared for the World Wide Fund for Nature. The Global Exchange for Social Investment, London

    Google Scholar 

  • Robinson D, Fitter A (1998) The magnitude and control of carbon transfer between plants linked by a common mycorrhizal network. J Exp Bot 50:9–13

    Article  Google Scholar 

  • Shen Q, Chu G (2004) Bi-directional nitrogen transfer in an intercropping system of peanut with rice cultivated in aerobic soil. Biol Fertil Soils 40:81–87

    Article  CAS  Google Scholar 

  • Singh MK, Parshad M, Arya RK, Kumar P, Ahlawat KS (2012) Performance of forage and legumes intercropping in Jatropha curcas plantation in semi-arid region of Haryana. Forage Res 38:86–90

    Google Scholar 

  • Skinner EM, Díaz-Pérez JC, Phatak SC, Schomberg HH, Vencill W (2012) Allelopathic effects of sunnhemp (Crotalaria juncea L.) on germination of vegetables and weeds. Hortic Sci 47:138–142

    Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal Symbiosis, 3rd edn. Academic Press, Elsevier, London

    Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Terren M, Cissé C, Mergeai G (2013) Analysis of the profitability prospects of the extensive cultivation of Jatropha curcas L. In the eastern transition agro-ecological zone of Senegal: the case of the rural community of Dialacoto. Cah Agric 22:568–574

    Google Scholar 

  • Teste FP, Veneklaas EJ, Dixon KW, Lambers H (2015) Is nitrogen transfer among plants enhanced by contrasting nutrient-acquisition strategies ? Plant Cell Environ 38:50–60

    Article  CAS  PubMed  Google Scholar 

  • Tomm GO, van Kessel C, Slinkard AE (1994) Bi-directional transfer of nitrogen between alfalfa and bromegrass: short and long term evidence. Plant Soil 164:77–86

    Article  CAS  Google Scholar 

  • Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Mesure du taux de mycorhization VA d’un système radiculaire. Recherche de méthodes d’estimation ayant une signification fonctionnelle. In: Gianinazzi-Pearson V, Gianinazzi S (eds) Mycorrhizae: physiology and genetics. INRA Press, Paris, pp. 217–221

    Google Scholar 

  • van der Heijden MGA, Horton TR (2009) Socialism in soil? The importance of mycorrhizal fungal networks for facilitation in natural ecosystems. J Ecol 97:1139–1150

    Article  Google Scholar 

  • Walder F, Nieman H, Natarajan M, Lehmann MF, Boller T, Wiemken A (2012) Mycorrhizal networks: common goods of plants shared under unequal terms of trade. Plant Physiol 159:789–797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang KH, Sipes BS, Schmitt DP (2002) Crotalaria as cover crop for nematode management: a review. Nematropica 32:35–57

    CAS  Google Scholar 

  • Yao Q, Li X, Ai W, Christie P (2003) Bi-directional transfer of phosphorus between red clover and perennial ryegrass via arbuscular mycorrhizal hyphal links. Eu J Soil Biol 39:47–54

    Article  CAS  Google Scholar 

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Acknowledgments

A. Dieng was supported by the IRD (Institut de Recherche pour le Développement).

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Authors and Affiliations

  1. IRD, UMR LSTM, 34398, Montpellier, France

    Amadou Dieng, Robin Duponnois & Ezékiel Baudoin

  2. Laboratoire Commun de Microbiologie IRD/ISRA/UCAD, Dakar, Sénégal

    Amadou Dieng & Ibrahima Ndoye

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  1. Amadou Dieng
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  2. Robin Duponnois
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  3. Ibrahima Ndoye
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  4. Ezékiel Baudoin
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Correspondence to Ezékiel Baudoin.

Electronic supplementary material

Online Resource 1

Sampling effort curves of the J. curcas and C. retusa root AMF diversity (PDF 88 kb)

Online Resource 2

Phylogenetic relationships of partial Glomeromycota 18S rDNA gene sequences amplified from J. curcas and C. retusa roots grown in J. curcas hedgerow (a) and fallow field (b) soils. Sequences are labeled from the left (e.g. 152-JS-1) according to the genotype identity number (e.g. 152), the modality (e.g. JS, with J or C in first position to identify J. curcas or C. retusa, followed by S, N and F for succession culture, no co-culture (jatropha sole crop) and co-culture, respectively), and the number of identical sequences (genotype size, e.g. 1). Neighbor-joining trees were rooted by ribosomal sequences of Endogone pisiformis and Mortierella polycephala as the outgroups. GenBank reference sequences are indicated with their accession numbers. Only bootstrap values ≥60 % (1000 replicates) are shown. Internal brackets delineate phylotypes. Scale bar: 1 % nucleotide substitution (PDF 141 kb)

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Dieng, A., Duponnois, R., Ndoye, I. et al. Positive feedback with mycorrhizal fungi alleviates negative effects of intercropping the energy crop Jatropha curcas with Crotalaria retusa . Symbiosis 73, 107–116 (2017). https://doi.org/10.1007/s13199-016-0459-y

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